THE BRAIN UNPLUGGED

"With the enormous advances made in the miniaturization of instruments, it is not unthinkable anymore that neuroethologists will, at one point in the future, be able to obtain physiological recordings from animals living a relatively normal life in their natural habitat!"
Gunther K.H. Zupanc, 2004

At least since the 1950s studies of sensory systems have been divided into two largely non-overlapping, perspectives: one is neuroethological, organismic, and concerned with understanding how the animal senses its environment and the brain’s role in guiding behavior. The other is neurophysiological: it tries to understand the function of neurons and connections in sensory circuits by probing them under well-controlled experimental conditions. Here the subject is typically anesthetized or restrained, connected by cables to laboratory equipment, and the stimuli are abstract and designed to favor subsequent mathematical analysis. Clearly these two strands will need to be unified some day, and indeed there has been a persistent trend in neurophysiology to work on awake animals and even allow them a degree of movement. We took a different approach, by bringing neurophysiology into the wild, as reported in this week’s Nature Neuroscience.

A new instrument allows us to observe brain function in unplugged animals moving freely in their natural habitat. Our design made use of components from very disparate domains: a commercial set of electrodes; a microchip based on circuits for the particle accelerator in Geneva; and a tiny transmitter developed for the needs of spies. The resulting miniature device compresses what used to be a man-sized rack of electronics into the palm of your hand, or – more importantly – onto the head of a rat. It records the voltage signals on 64 brain electrodes, amplifies and processes them, and radios the result to a remote receiver up to 100 m away. It is light enough to allow the rat full freedom of movement, and runs for 6 hours on a single battery charge.

Much of our report is concerned with pleasing the skeptics, documenting the technical capabilities of the wireless recorder, and testing it in the laboratory against conventional recording systems under a wide range of experimental conditions. The quality of the wireless recordings is in fact indistinguishable from state-of-the-art wired systems. We expect that this technology will soon replace the cumbersome and expensive rack-mounted instruments with cables, even under conditions that don’t require full mobility of the animal.

But the most satisfying and exciting experiments happened when we released our rats into the wild: not quite the jungle perhaps, but a large enclosure at the Concord Field Station. The animals were fully engaged with this rich environment. No need for the frequent rat-naps that one observes in constrained laboratory conditions! Rats explored the field, built nests, and burrowed. Not wanting to wait for them to complete a tunnel on their own, we provided some pre-fab pipes that proved popular.

In our first experiments we aimed electrodes at the primary visual cortex, an early processing station along the visual pathway, and recorded the trains of action potentials from multiple neurons in parallel. Many of the cells were strongly modulated in their firing in ways that correlated with the animal’s behavior, for example as the rat emerged from a pipe, or as it explored the leaf litter. Clearly every movement of the animal brings a new scene into view, and this drives the visual pathways. Altogether we were surprised how much of the activity in a presumed “visual” region of the brain can be predicted by simply watching the animal move. In ongoing work we want to explore further the nature of these sensory-motor loops that characterize the animal’s natural behavior, and understand to what extent the insights from laboratory-bound experiments translate into the wild.